Animal,but not human,faces engage the distributed face network in adolescents with autism

Multiple hypotheses have been offered to explain the impaired face‐processing behavior and the accompanying underlying disruptions in neural circuitry among individuals with autism. We explored the specificity of atypical face‐processing activation and potential alterations to fusiform gyrus (FG) morphology as potential underlying mechanisms. Adolescents with high functioning autism (HFA) and age‐matched typically developing (TD) adolescents were scanned with sMRI and fMRI as they observed human and animal faces. In spite of exhibiting comparable face recognition behavior, the HFA adolescents evinced hypo‐activation throughout the face‐processing system in response to unfamiliar human, but not animal, faces. They also exhibited greater activation in affective regions of the face‐processing network in response to animal, but not human, faces. Importantly, this atypical pattern of activation in response to human faces was not related to atypical structural properties of the FG. This atypical neural response to human faces in autism may stem from abnormalities in the ability to represent the reward value of social (i.e. conspecific) stimuli.     

Reduced Reliance on Optimal Facial Information for Identity Recognition in Autism Spectrum Disorder

Previous research into face processing in autism spectrum disorder (ASD) has revealed atypical biases toward particular facial information during identity recognition. Specifically, a focus on features (or high spatial frequencies [HSFs]) has been reported for both face and nonface processing in ASD. The current study investigated the development of spatial frequency biases in face recognition in children and adolescents with and without ASD, using nonverbal mental age to assess changes in biases over developmental time. Using this measure, the control group showed a gradual specialization over time toward middle spatial frequencies (MSFs), which are thought to provide the optimal information for face recognition in adults. By contrast, individuals with ASD did not show a bias to one spatial frequency band at any stage of development. These data suggest that the “midband bias” emerges through increasing face-specific experience and that atypical face recognition performance may be related to reduced specialization toward optimal spatial frequencies in ASD.     

The study of autism as a distributed disorder

Past autism research has often been dedicated to tracing the causes of the disorder to a localized neurological abnormality, a single functional network, or a single cognitive-behavioral domain. In this review, I argue that autism is a "distributed disorder" on various levels of study (genetic, neuroanatomical, neurofunctional, behavioral). "Localizing" models are therefore not promising. The large array of potential genetic risk factors suggests that multiple (or all) emerging functional brain networks are affected during early development. This is supported by widespread growth abnormalities throughout the brain. Interactions during development between affected functional networks and atypical experiential effects (associated with atypical behavior) in children with autism further complicate the neurological bases of the disorder, resulting in an "exponentially distributed" profile. Promising approaches to a better characterization of neural endophenotypes in autism are provided by techniques investigating white matter and connectivity, such as MR spectroscopy, diffusion-tensor imaging (DTI), and functional connectivity MRI. According to a recent hypothesis, the autistic brain is generally characterized by "underconnectivity." However, not all findings are consistent with this view. The concepts and methodology of functional connectivity need to be refined and results need to be corroborated by anatomical studies (such as DTI tractography) before definitive conclusions can be drawn.     

Face engagement during infancy predicts later face recognition ability in younger siblings of children with autism

Face recognition difficulties are frequently documented in children with autism spectrum disorders (ASD). It has been hypothesized that these difficulties result from a reduced interest in faces early in life, leading to decreased cortical specialization and atypical development of the neural circuitry for face processing. However, a recent study by our lab demonstrated that infants at increased familial risk for ASD, irrespective of their diagnostic status at 3 years, exhibit a clear orienting response to faces. The present study was conducted as a follow‐up on the same cohort to investigate how measures of early engagement with faces relate to face‐processing abilities later in life. We also investigated whether face recognition difficulties are specifically related to an ASD diagnosis, or whether they are present at a higher rate in all those at familial risk. At 3 years we found a reduced ability to recognize unfamiliar faces in the high‐risk group that was not specific to those children who received an ASD diagnosis, consistent with face recognition difficulties being an endophenotype of the disorder. Furthermore, we found that longer looking at faces at 7 months was associated with poorer performance on the face recognition task at 3 years in the high‐risk group. These findings suggest that longer looking at faces in infants at risk for ASD might reflect early face‐processing difficulties and predicts difficulties with recognizing faces later in life.     

Individual differences in holistic processing predict face recognition ability

Why do some people recognize faces easily and others frequently make mistakes in recognizing faces? Classic behavioral work has shown that faces are processed in a distinctive holistic manner that is unlike the processing of objects. In the study reported here, we investigated whether individual differences in holistic face processing have a significant influence on face recognition. We found that the magnitude of face-specific recognition accuracy correlated with the extent to which participants processed faces holistically, as indexed by the composite-face effect and the whole-part effect. This association is due to face-specific processing in particular, not to a more general aspect of cognitive processing, such as general intelligence or global attention. This finding provides constraints on computational models of face recognition and may elucidate mechanisms underlying cognitive disorders, such as prosopagnosia and autism, that are associated with deficits in face recognition.     

A cross-syndrome study of the development of holistic face recognition in children with autism, Down syndrome, and Williams syndrome

We report a cross-syndrome comparison of the development of holistic processing in face recognition in school-aged children with developmental disorders: autism, Down syndrome, and Williams syndrome. The autism group was split into two groups: one with high-functioning children and one with low-functioning children. The latter group has rarely been studied in this context. The four disorder groups were compared with typically developing children. Cross-sectional trajectory analyses were used to compare development in a modified version of Tanaka and Farah’s part–whole task. Trajectories were constructed linking part–whole performance either to chronological age or to several measures of mental age (receptive vocabulary, visuospatial construction, and the Benton Facial Recognition Test). In addition to variable delays in onset and rate of development, we found an atypical profile in all disorder groups. These profiles were atypical in different ways, indicating multiple pathways to, and variable outcomes in, the development of face recognition. We discuss the implications for theories of face recognition in both atypical and typical development, including the idea that part–whole and rotation manipulations may tap different aspects of holistic and/or configural processing.     

Functional connectivity differences in autism during face and car recognition: underconnectivity and atypical age‐related changes

Face recognition abilities improve between adolescence and adulthood over typical development (TD), but plateau in autism, leading to increasing face recognition deficits in autism later in life. Developmental differences between autism and TD may reflect changes between neural systems involved in the development of face encoding and recognition. Here, we focused on whole‐brain connectivity with the fusiform face area (FFA), a well‐established face‐preferential brain region. Older children, adolescents, and adults with and without autism completed the Cambridge Face Memory Test, and a matched car memory test, during fMRI scanning. We then examined task‐based functional connectivity between the FFA and the rest of the brain, comparing autism and TD groups during encoding and recognition of face and car stimuli. The autism group exhibited underconnectivity, relative to the TD group, between the FFA and frontal and primary visual cortices, independent of age. Underconnectivity with the medial and rostral lateral prefrontal cortex was face‐specific during encoding and recognition, respectively. Conversely, underconnectivity with the L orbitofrontal cortex was evident for both face and car encoding. Atypical age‐related changes in connectivity emerged between the FFA and the R temporoparietal junction, and R dorsal striatum for face stimuli only. Similar differences in age‐related changes in autism emerged for FFA connectivity with the amygdala across both face and car recognition. Thus, underconnectivity and atypical development of functional connectivity may lead to a less optimal face‐processing network in the context of increasing general and social cognitive deficits in autism.     

A connectionist model of category learning by individuals with high-functioning autism spectrum disorder

Individuals with autism spectrum disorder (ASD) show atypical patterns of learning and generalization. We explored the possible impacts of autism-related neural abnormalities on perceptual category learning using a neural network model of visual cortical processing. When applied to experiments in which children or adults were trained to classify complex two-dimensional images, the model can account for atypical patterns of perceptual generalization. This is only possible, however, when individual differences in learning are taken into account. In particular, analyses performed with a self-organizing map suggested that individuals with high-functioning ASD show two distinct generalization patterns: one that is comparable to typical patterns, and a second in which there is almost no generalization. The model leads to novel predictions about how individuals will generalize when trained with simplified input sets and can explain why some researchers have failed to detect learning or generalization deficits in prior studies of category learning by individuals with autism. On the basis of these simulations, we propose that deficits in basic neural plasticity mechanisms may be sufficient to account for the atypical patterns of perceptual category learning and generalization associated with autism, but they do not account for why only a subset of individuals with autism would show such deficits. If variations in performance across subgroups reflect heterogeneous neural abnormalities, then future behavioral and neuroimaging studies of individuals with ASD will need to account for such disparities.     

Facial Emotion Recognition in Autism Spectrum Disorders: A Review of Behavioral and Neuroimaging Studies

Behavioral studies of facial emotion recognition (FER) in autism spectrum disorders (ASD) have yielded mixed results. Here we address demographic and experiment-related factors that may account for these inconsistent findings. We also discuss the possibility that compensatory mechanisms might enable some individuals with ASD to perform well on certain types of FER tasks in spite of atypical processing of the stimuli, and difficulties with real-life emotion recognition. Evidence for such mechanisms comes in part from eye-tracking, electrophysiological, and brain imaging studies, which often show abnormal eye gaze patterns, delayed event-related-potential components in response to face stimuli, and anomalous activity in emotion-processing circuitry in ASD, in spite of intact behavioral performance during FER tasks. We suggest that future studies of FER in ASD: 1) incorporate longitudinal (or cross-sectional) designs to examine the developmental trajectory of (or age-related changes in) FER in ASD and 2) employ behavioral and brain imaging paradigms that can identify and characterize compensatory mechanisms or atypical processing styles in these individuals.     

Exploring face perception in disorders of development: Evidence from Williams syndrome and autism

Individuals with Williams syndrome (WS) and autism are characterized by different social phenotypes but have been said to show similar atypicalities of face‐processing style. Although the structural encoding of faces may be similarly atypical in these two developmental disorders, there are clear differences in overall face skills. The inclusion of both populations in the same study can address how the profile of face skills varies across disorders. The current paper explored the processing of identity, eye‐gaze, lip‐reading, and expressions of emotion using the same participants across face domains. The tasks had previously been used to make claims of a modular structure to face perception in typical development. Participants with WS (N=15) and autism (N=20) could be dissociated from each other, and from individuals with general developmental delay, in the domains of eye‐gaze and expression processing. Individuals with WS were stronger at these skills than individuals with autism. Even if the structural encoding of faces appears similarly atypical in these groups, the overall profile of face skills, as well as the underlying architecture of face perception, varies greatly. The research provides insights into typical and atypical models of face perception in WS and autism.     

Early processing of emotional faces in children with autism: An event-related potential study

Social deficits are one of the most striking manifestations of autism spectrum disorders (ASDs). Among these social deficits, the recognition and understanding of emotional facial expressions has been widely reported to be affected in ASDs. We investigated emotional face processing in children with and without autism using event-related potentials (ERPs). High-functioning children with autism (n = 15, mean age = 10.5 ± 3.3 years) completed an implicit emotional task while visual ERPs were recorded. Two groups of typically developing children (chronological age-matched and verbal equivalent age-matched [both ns = 15, mean age = 7.7 ± 3.8 years]) also participated in this study. The early ERP responses to faces (P1 and N170) were delayed, and the P1 was smaller in children with autism than in typically developing children of the same chronological age, revealing that the first stages of emotional face processing are affected in autism. However, when matched by verbal equivalent age, only P1 amplitude remained affected in autism. Our results suggest that the emotional and facial processing difficulties in autism could start from atypicalities in visual perceptual processes involving rapid feedback to primary visual areas and subsequent holistic processing.     

Emotional face recognition in autism and in cerebral visual impairments: In search for specificity

Autism spectrum disorder (ASD) is characterized by difficulties in the social domain, but also by hyper- and hypo-reactivity. Atypical visual behaviours and processing have often been observed. Nevertheless, several similar signs are also identified in other clinical conditions including cerebral visual impairments (CVI). In the present study, we investigated emotional face categorization in groups of children with ASD and CVI by comparing each group to typically developing individuals (TD) in two tasks. Stimuli were either non-filtered or filtered by low- and high-spatial frequencies (LSF and HSF). All participants completed the autism spectrum quotient score (AQ) and a complete neurovisual evaluation. The results show that while both clinical groups presented difficulties in the emotional face recognition tasks and atypical processing of filtered stimuli, they did not differ from one another. Additionally, autistic traits were observed in the CVI group and symmetrically, some visual disturbances were present in the ASD group as measured via the AQ score and a neurovisual evaluation, respectively. The present study suggests the relevance of comparing ASD to CVI by showing that emotional face categorization difficulties should not be solely considered as autism-specific but merit investigation for potential dysfunction of the visual processing neural network. These results are of interest in both clinical and research perspectives, indicating that systematic visual examination is warranted for individuals with ASD.     

Evidence for reduced domain-specificity in auditory processing in autism

Neurological and behavioral findings indicate that atypical auditory processing characterizes autism. The present study tested the hypothesis that auditory processing is less domain-specific in autism than in typical development. Participants with autism and controls completed a pitch sequence discrimination task in which same/different judgments of music and/or speech stimulus pairs were made. A signal detection analysis showed no difference in pitch sensitivity across conditions in the autism group, while controls exhibited significantly poorer performance in conditions incorporating speech. The results are largely consistent with perceptual theories of autism, which propose that a processing bias towards featural/low-level information characterizes the disorder, as well as supporting the notion that such individuals exhibit selective attention to a limited number of simultaneously presented cues.     

自我面孔识别的独特性

与识别他人的面孔相比,自我面孔识别在行为反应、种系发生、个体发展以及脑机制等方面都具有很大的独特性。行为指标方面,自我面孔识别在速度上快于识别他人的面孔;种系发生方面,只有人类和大猩猩等高级灵长类动物才具有识别自己面孔的能力;个体发展方面,儿童出生后不久即能识别他人面孔,但要在18个月左右才能表现出自我面孔识别能力;脑机制方面,神经心理学和脑成像研究结果表明自我面孔识别可能主要是右脑的功能。该领域的研究进展将为深入了解自我的形成机理提供一个新的探视“窗口”。     

The “parts and wholes” of face recognition: A review of the literature

It has been claimed that faces are recognized as a “whole” rather than by the recognition of individual parts. In a paper published in the Quarterly Journal of Experimental Psychology in 1993, Martha Farah and I attempted to operationalize the holistic claim using the part/whole task. In this task, participants studied a face and then their memory presented in isolation and in the whole face. Consistent with the holistic view, recognition of the part was superior when tested in the whole-face condition compared to when it was tested in isolation. The “whole face” or holistic advantage was not found for faces that were inverted, or scrambled, nor for non-face objects, suggesting that holistic encoding was specific to normal, intact faces. In this paper, we reflect on the part/whole paradigm and how it has contributed to our understanding of what it means to recognize a face as a “whole” stimulus. We describe the value of part/whole task for developing theories of holistic and non-holistic recognition of faces and objects. We discuss the research that has probed the neural substrates of holistic processing in healthy adults and people with prosopagnosia and autism. Finally, we examine how experience shapes holistic face recognition in children and recognition of own- and other-race faces in adults. The goal of this article is to summarize the research on the part/whole task and speculate on how it has informed our understanding of holistic face processing.     

Developmental plateau in visual object processing from adolescence to adulthood in autism

A lack of typical age-related improvement from adolescence to adulthood contributes to face recognition deficits in adults with autism on the Cambridge Face Memory Test (CFMT). The current studies examine if this atypical developmental trajectory generalizes to other tasks and objects, including parts of the face. The CFMT tests recognition of whole faces, often with a substantial delay. The current studies used the immediate memory (IM) task and the parts-whole face task from the Let’s Face It! battery, which examines whole faces, face parts, and cars, without a delay between memorization and test trials. In the IM task, participants memorize a face or car. Immediately after the target disappears, participants identify the target from two similar distractors. In the part-whole task, participants memorize a whole face. Immediately after the face disappears, participants identify the target from a distractor with different eyes or mouth, either as a face part or a whole face.Results indicate that recognition deficits in autism become more robust by adulthood, consistent with previous work, and also become more general, including cars. In the IM task, deficits in autism were specific to faces in childhood, but included cars by adulthood. In the part-whole task, deficits in autism became more robust by adulthood, including both eyes and mouths as parts and in whole faces. Across tasks, the deficit in autism increased between adolescence and adulthood, reflecting a lack of typical improvement, leading to deficits with non-face stimuli and on a task without a memory delay. These results suggest that brain maturation continues to be affected into adulthood in autism, and that the transition from adolescence to adulthood is a vulnerable stage for those with autism.     

Mechanisms of developmental regression in autism and the broader phenotype: a neural network modeling approach

Loss of previously established behaviors in early childhood constitutes a markedly atypical developmental trajectory. It is found almost uniquely in autism and its cause is currently unknown (Baird et al., 2008). We present an artificial neural network model of developmental regression, exploring the hypothesis that regression is caused by overaggressive synaptic pruning and identifying the mechanisms involved. We used a novel population-modeling technique to investigate developmental deficits, in which both neurocomputational parameters and the learning environment were varied across a large number of simulated individuals. Regression was generated by the atypical setting of a single pruning-related parameter. We observed a probabilistic relationship between the atypical pruning parameter and the presence of regression, as well as variability in the onset, severity, behavioral specificity, and recovery from regression. Other neurocomputational parameters that varied across the population modulated the risk that an individual would show regression. We considered a further hypothesis that behavioral regression may index an underlying anomaly characterizing the broader autism phenotype. If this is the case, we show how the model also accounts for several additional findings: shared gene variants between autism and language impairment (Vernes et al., 2008); larger brain size in autism but only in early development (Redcay & Courchesne, 2005); and the possibility of quasi-autism, caused by extreme environmental deprivation (Rutter et al., 1999). We make a novel prediction that the earliest developmental symptoms in the emergence of autism should be sensory and motor rather than social and review empirical data offering preliminary support for this prediction.     

高功能自闭症个体对威胁性情绪面孔的注意偏向

高功能自闭症(High-Functioning Autism, HFA)个体智力正常, 但也面临着严重的社会功能障碍。对威胁性情绪面孔的注意偏向与HFA个体社会功能的发展密切相关。梳理相关研究发现, HFA个体在自动加工阶段和情绪目标参与阶段, 不存在威胁性情绪面孔注意偏向; 而在任务与情绪无关的控制加工阶段, 存在威胁性情绪面孔注意偏向。针对HFA个体威胁性情绪面孔注意偏向的理论解释主要有杏仁核理论、强烈世界理论和执行功能理论等。神经生理机制方面, HFA个体对威胁性情绪面孔的注意偏向可能与其异常的皮下及皮层通路功能有关, 同时可能会受5-羟色胺系统基因及催产素水平等的影响。未来研究可在综合考虑研究方法及个体因素的基础上, 进一步探究其加工特征及神经生物机制, 着力开发科学有效的干预策略。     

fNIRS在自闭症脑功能研究中的应用与展望

社会交往能力是人类生存的基本技能。社交能力的缺失会导致严重的行为障碍和精神疾病,如自闭症。由于自闭症儿童的特殊性,绝大多数的自闭症脑成像研究多集中在年龄较大的高功能自闭症儿童在静息态或简单的任务态下的脑激活模式或功能连接状态。自闭症的核心症状—社会交往障碍和语言交流障碍却较少有研究触及。近年来,近红外光学脑功能成像技术的发展为我们在真实的交流和互动中研究自闭症儿童的神经病理机制提供了新的工具和机遇。     

The neural underpinnings of prosody in autism

This study examines the processing of prosodic cues to linguistic structure and to affect, drawing on fMRI and behavioral data from 16 high-functioning adolescents with autism spectrum disorders (ASD) and 11 typically developing controls. Stimuli were carefully matched on pitch, intensity, and duration, while varying systematically in conditions of affective prosody (angry versus neutral speech) and grammatical prosody (questions versus statement). To avoid conscious attention to prosody, which normalizes responses in young people with ASD, the implicit comprehension task directed attention to semantic aspects of the stimuli. Results showed that when perceiving prosodic cues, both affective and grammatical, activation of neural regions was more generalized in ASD than in typical development, and areas recruited reflect heightened reliance on cognitive control, reading of intentions, attentional management, and visualization. This broader recruitment of executive and "mind-reading" brain areas for a relative simple language-processing task may be interpreted to suggest that speakers with high-functioning autism (HFA) have developed less automaticity in language processing and may also suggest that "mind-reading" or theory of mind deficits are intricately bound up in language processing. Data provide support for both a right-lateralized as well as a bilateral model of prosodic processing in typical individuals, depending upon the function of the prosodic information.